Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens

• Published in: Parasites & vectors Vol. 11; no. 1; p. 600
• Main Authors: Hofmeester, Tim R., Krawczyk, Aleksandra I., van Leeuwen, Arieke Docters, Fonville, Manoj, Montizaan, Margriet G. E., van den Berge, Koen, Gouwy, Jan, Ruyts, Sanne C., Verheyen, Kris, Sprong, Hein
• Format: Journal Article
• Language: English
• Published: London BioMed Central 20.11.2018; BMC
• Subjects: Anaplasma phagocytophilum; Anaplasma phagocytophilum - genetics; Anaplasma phagocytophilum - isolation & purification; Anaplasma phagocytophilum - pathogenicity; Anaplasmataceae - genetics; Anaplasmataceae - isolation & purification; Anaplasmataceae - pathogenicity; Animals; Animals, Wild; Arachnids; Badgers; Belgium; Belgium - epidemiology; Biomedical and Life Sciences; Biomedicine; Body organs; Borrelia burgdorferi; Borrelia burgdorferi (s.l.); Borrelia burgdorferi - genetics; Borrelia burgdorferi - isolation & purification; Borrelia burgdorferi - pathogenicity; Borrelia Infections - transmission; Borrelia Infections - veterinary; Borrelia miyamotoi; Cycles; Deoxyribonucleic acid; DNA; DNA, Bacterial - chemistry; DNA, Bacterial - genetics; DNA, Bacterial - isolation & purification; Ehrlichiosis - complications; Ehrlichiosis - epidemiology; Ehrlichiosis - transmission; Ehrlichiosis - veterinary; Entomology; enzootic diseases; Feeding; Ferrets - microbiology; Forces (mechanics); Hedgehogs - parasitology; hosts; Infectious Diseases; Ixodes - microbiology; Ixodes hexagonus; Ixodes ricinus; Larvae; Life Cycle Stages; Lyme disease; Lyme Disease - epidemiology; Lyme Disease - microbiology; Lyme Disease - transmission; Lyme Disease - veterinary; Martes foina; Martes martes; Meles meles; Mustela putorius; Mustelidae; Mustelidae - parasitology; Neoehrlichia mikurensis; Netherlands; Netherlands - epidemiology; Nymph - microbiology; Nymphs; Organs; Parasitic diseases; Parasitology; Pathogens; Pine; Rickettsia - genetics; Rickettsia - isolation & purification; Rickettsia - pathogenicity; Species; Tick Infestations - complications; Tick Infestations - epidemiology; Tick Infestations - veterinary; Tick-borne diseases; Tick-Borne Diseases - microbiology; Tick-Borne Diseases - transmission; Tick-Borne Diseases - veterinary; Ticks; Tropical Medicine; Vectors (Biology); Veterinary Medicine/Veterinary Science; Virology; Wildlife; Zoonoses; Belgium; Netherlands; Europe; (; ); Anaplasma phagocytophilum; Ixodes hexagonus; Martes martes; Meles meles; Borrelia miyamotoi; Borrelia burgdorferi (s.l.); Ixodes ricinus; Martes foina; Mustela putorius; Neoehrlichia mikurensis
• ISSN: 1756-3305; 1756-3305
• DOI: 10.1186/s13071-018-3126-8

Background Elucidating which wildlife species significantly contribute to the maintenance of Ixodes ricinus populations and the enzootic cycles of the pathogens they transmit is imperative in understanding the driving forces behind the emergence of tick-borne diseases. Here, we aimed to quantify the relative contribution of four mustelid species in the life-cycles of I. ricinus and Borrelia burgdorferi ( sensu lato ) in forested areas and to investigate their role in the transmission of other tick-borne pathogens . Road-killed badgers, pine martens, stone martens and polecats were collected in Belgium and the Netherlands. Their organs and feeding ticks were tested for the presence of tick-borne pathogens. Results Ixodes hexagonus and I. ricinus were found on half of the screened animals ( n = 637). Pine martens had the highest I. ricinus burden, whereas polecats had the highest I. hexagonus burden. We detected DNA from B. burgdorferi ( s.l. ) and Anaplasma phagocytophilum in organs of all four mustelid species ( n = 789), and Neoehrlichia mikurensis DNA was detected in all species, except badgers. DNA from B. miyamotoi was not detected in any of the investigated mustelids. From the 15 larvae of I. ricinus feeding on pine martens ( n = 44), only one was positive for B. miyamotoi DNA, and all tested negative for B. burgdorferi ( s.l. ), N. mikurensis and A. phagocytophilum . The two feeding larvae from the investigated polecats ( n = 364) and stone martens ( n = 39) were negative for all four pathogens. The infection rate of N. mikurensis was higher in feeding nymphs collected from mustelids compared to questing nymphs, but not for B. burgdorferi ( s.l. ), B. miyamotoi or A. phagocytophilum. Conclusions Although all stages of I. ricinus can be found on badgers, polecats, pine and stone martens, their relative contribution to the life-cycle of I. ricinus in forested areas is less than 1%. Consequently, the relative contribution of mustelids to the enzootic cycles of I. ricinus -borne pathogens is negligible, despite the presence of these pathogens in organs and feeding ticks. Interestingly, all four mustelid species carried all stages of I. hexagonus , potentially maintaining enzootic cycles of this tick species apart from the cycle involving hedgehogs as main host species.